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Evolution of the Eukaryotic Membrane-Trafficking System

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Evolution of the Eukaryotic Membrane-Trafficking System Downloaded from http://cshperspectives.cshlp.org/ on September 26, 2021 - Published by Cold Spring Harbor Laboratory Press Missing Pieces of an Ancient Puzzle: Evolution of the Eukaryotic Membrane-Trafficking System Alexander Schlacht1, Emily K. Herman1, Mary J. Klute1, Mark C. Field2, and Joel B. Dacks1 1Department of Cell Biology, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Alberta T6G 2H7, Canada 2Division of Biological Chemistry and Drug Discovery, University of Dundee, Dundee, Scotland DD1 5EH, United Kingdom Correspondence: [email protected] The membrane-trafficking system underpins cellular trafficking of material in eukaryotes and its evolution would have been a watershed in eukaryogenesis. Evolutionary cell biological studies have been unraveling the history of proteins responsible for vesicle transport and organelle identity revealing both highly conserved components and lineage-specific inno- vations. Recently, endomembrane components with a broad, but patchy, distribution have been observed as well, pieces that are missing from our cell biological and evolutionary models of membrane trafficking. These data together allow for new insights into the history and forces that shape the evolution of this critical cell biological system. major feature of eukaryotic cells is subcom- hanced the ability of even the earliest eukaryotes Apartmentalization. Specific components are to remodel their cell surface, export proteins concentrated within restricted regions of the to modify their external environment by exocy- cell, necessitating the presence of one or more tosis, as well as acquire nutrients by endocyto- targeting mechanisms. The eukaryotic mem- sis. Subcompartmentalization of the cell and brane-trafficking system facilitates intracellular the ability to direct material to specific com- transport of proteins and lipids between organ- partments would have allowed for intracellular elles and further acts to build the interface be- specializations, for example, the sequestration tween the cell and external environment. This of metabolic processes. Membrane trafficking system touches, at some level, virtually every also likelyserved to integrate fledgling endosym- cellular compartment and component; its prop- biotic interactions (Flinneret al. 2013; Wideman er function is crucial for modern eukaryotes. et al. 2013), regardless of the precise timing of The establishment of the membrane-traf- the mitochondrial endosymbiotic event with re- ficking system represented a tremendous mile- spect to the evolution of endogenously derived stone in the restructuring that took place during organelles (Martin and Muller 1998; Cavalier- the transition from the prokaryotic to eukaryot- Smith 2002; Martin and Koonin 2006; Forterre ic cellular configuration. As it does today, a 2011). Finally, trafficking could have also facili- membrane-trafficking system would have en- tated a size increase for the proto-eukaryotic Editors: Patrick J. Keeling and Eugene V. Koonin Additional Perspectives on The Origin and Evolution of Eukaryotes available at www.cshperspectives.org Copyright # 2014 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a016048 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016048 1 Downloaded from http://cshperspectives.cshlp.org/ on September 26, 2021 - Published by Cold Spring Harbor Laboratory Press A. Schlacht et al. organisms and enabled their colonization of body, trans-Golgi network (TGN), varioustypes novel ecological niches; for example, phagocy- of endolysosomal organelles (early, recycling, tosis is a critical function that would have been and late endosomes and lysosomes/vacuoles), made possible by this change in morphology. as well as the plasma membrane (Fig. 1A). How- In the textbook definition (e.g., Alberts ever, recent work has uncovered greater inte- 2002), the membrane-trafficking system con- gration between these classical membrane-traf- sists of the endoplasmic reticulum, the Golgi ficking compartments and other organelles Plasma membrane A Golgi stack Exocytosis Flagellum Nucleus Recycling endosome Endocytosis Phagocytosis Lysosome Late endosome/MVB Early endosome BC Organelle paralogy hypothesis Rab Coat Modern protein SNARE complexes Assembly Disassembly Primordial complex Figure 1. Eukaryotic endomembrane organelles and evolution. (A) A eukaryotic cell depicting the major endomembrane organelles and trafficking pathways (denoted by arrows). Figure created from data in Wideman et al. (2013). (B) Depiction of specificity machinery encoded by multiple components of the vesicle formation and fusion machinery. For diagrammatic simplicity only the Coats, Rabs, and SNAREs are shown. (C) The organelle paralogy hypothesis for the evolution of novel endomembrane organelles by duplication and coevo- lution of identity-encoding genes. 2 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016048 Downloaded from http://cshperspectives.cshlp.org/ on September 26, 2021 - Published by Cold Spring Harbor Laboratory Press Evolution of the Endomembrane System including the nucleus (Dokudovskaya et al. organelles, and with the diversity of eukaryot- 2009), peroxisomes (Agrawal and Subramani ic organisms possessing membrane-traffick- 2013), and even the endosymbiotic organelles, ing machinery, understanding the processes of particularly the mitochondria (Braschi et al. transport specificity and organelle identity ben- 2010; Michel and Kornmann 2012; Sandoval efits from a more holistic view. and Simmen 2012). Although the molecular de- Evolutionary cell biology, one aspect of tails of the latter are still being unearthed, much which is the application of comparative molec- insight has been gained into the processes of ular evolutionary analysis to cell biology (Brod- transport between membrane-trafficking or- sky et al. 2012), is particularly valuable in ganelles by vesicle formation and the subsequent addressing such sweeping questions. Using a deliveryand fusion of the transport vesiclewith a toolkit comprising comparative genomics, mo- target organelle. lecular phylogenetics, and, more recently, math- The core molecular machinery for transport ematical modeling, it has been possible to re- between endomembrane organelles consists of construct the characteristics and complements proteins and lipids that must, in a combinatori- of the membrane-trafficking machinery in early al manner, encode the information required eukaryotic ancestors. Importantly, it has been for transport specificity (Cai et al. 2007). The possible to validate some of these in silico pre- generally accepted model for packaging of ma- dictions of function and behavior of protein terial into vesicles at a given organelle involves components through molecular cell biological GTPases of the Arf/Sar family, along with a characterization in model eukaryotes beyond number of activating and effector proteins (Bo- mammals and yeast. This provides increased nifacino and Glick 2004). Further to this is a confidence in predictions of ancient mem- requirement for cargo selection, membrane de- brane-trafficking systems, rather than being formation, and scission involving one or more solely reliant on deduced histories of protein coat protein complexes (COPI, COPII, clathrin/ families. Furthermore, by considering the evo- adaptins, ESCRTs, retromer) to generate the lutionary histories of trafficking components as transport carriers. Delivery of the carrier ini- an integrated set or cohort, it has been possible tially involves a tethering step involving Rab to begin deriving mechanistic models of how GTPases, and their modulating GTPase-activat- nonendosymbiotic organelles may evolve. In- ing proteins (GAPs) and guanine nucleotide terestingly, as surveys have advanced in scope, exchange factors, as well as multisubunit tether- some unexpected patterns of conservation have ing complexes (MTCs). The final fusion be- begun to emerge in the machinery of membrane tween the transport carrier and target organelle trafficking that have shed light on the evolution involves additional protein families such as of the system, but also raised questions as to the SNAREs and SM proteins (Bonifacino and Glick processes that have shaped it. 2004). Increasingly, the lines between these var- ious sets of machineries have been blurring, with complexes being identified composed of a mix- A SOPHISTICATED ANCIENT MEMBRANE- ture of proteins initially identified as involved in TRAFFICKING MACHINERY AND AN either vesicle formation or fusion (e.g., Miller EVOLUTIONARY MECHANISM OF NONENDOSYMBIOTIC et al. 2007; Pryor et al. 2008). To add a level of ORGANELLE EVOLUTION complexity, many of the aforementioned pro- teins are, in fact, protein families in which each The availability of genome sequences from di- paralog performs the same mechanistic role, verse eukaryotic organisms, and the tools to but at defined organelles or transport pathways sensitively identify genes common between ge- within the cell (Bonifacino and Glick 2004). nomes, have allowed evolutionary investiga- With the number of individual components in- tions into the history of the membrane-traffick- volved in the membrane-trafficking process, the ing system back to more than two billion years interconnectivity between the machineries and ago. The most tractable point of reconstruction Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016048 3 Downloaded from http://cshperspectives.cshlp.org/ on September 26, 2021 - Published by Cold Spring Harbor Laboratory Press A. Schlacht
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